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Erschienen in: Brain Structure and Function 5/2015

01.09.2015 | Original Article

The strength of weak connections in the macaque cortico-cortical network

verfasst von: Alexandros Goulas, Alexander Schaefer, Daniel S. Margulies

Erschienen in: Brain Structure and Function | Ausgabe 5/2015

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Abstract

Examination of the cortico-cortical network of mammals has unraveled key topological features and their role in the function of the healthy and diseased brain. Recent findings from social and biological networks pinpoint the significant role of weak connections in network coherence and mediation of information from segregated parts of the network. In the current study, inspired by such findings and proposed architectures pertaining to social networks, we examine the structure of weak connections in the macaque cortico-cortical network by employing a tract-tracing dataset. We demonstrate that the cortico-cortical connections as a whole, as well as connections between segregated communities of brain areas, comply with the architecture suggested by the so-called strength-of-weak-ties hypothesis. However, we find that the wiring of these connections is not optimal with respect to the aforementioned architecture. This configuration is not attributable to a trade-off with factors known to constrain brain wiring, i.e., wiring cost and efficiency. Lastly, weak connections, but not strong ones, appear important for network cohesion. Our findings relate a topological property to the strength of cortico-cortical connections, highlight the prominent role of weak connections in the cortico-cortical structural network and pinpoint their potential functional significance. These findings suggest that certain neuroimaging studies, despite methodological challenges, should explicitly take them into account and not treat them as negligible.
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Literatur
Zurück zum Zitat Bezgin G, Vakorin VA, van Opstal AJ, McIntosh AR, Bakker R (2012) Hundreds of brain maps in one atlas: registering coordinate-independent primate neuro-anatomical data to a standard brain. Neuroimage 62:67–76CrossRefPubMed Bezgin G, Vakorin VA, van Opstal AJ, McIntosh AR, Bakker R (2012) Hundreds of brain maps in one atlas: registering coordinate-independent primate neuro-anatomical data to a standard brain. Neuroimage 62:67–76CrossRefPubMed
Zurück zum Zitat Bota M, Swanson LW (2010) Collating and curating neuroanatomical nomenclatures: principles and use of the Brain Architecture Knowledge Management System (BAMS). Front Neuroinform 4:3PubMedCentralPubMed Bota M, Swanson LW (2010) Collating and curating neuroanatomical nomenclatures: principles and use of the Brain Architecture Knowledge Management System (BAMS). Front Neuroinform 4:3PubMedCentralPubMed
Zurück zum Zitat Broder A, Kumar R, Maghoul F, Raghavan P, Rajagopalan S, Stata R, Tomkins A, Wiener J (2000) Graph structure in the web. Comput Netw 33:309–320CrossRef Broder A, Kumar R, Maghoul F, Raghavan P, Rajagopalan S, Stata R, Tomkins A, Wiener J (2000) Graph structure in the web. Comput Netw 33:309–320CrossRef
Zurück zum Zitat Chen Y, Wang S, Hilgetag CC, Zhou C (2013) Trade-off between multiple constraints enables simultaneous formation of modules and hubs in neural systems. PLoS Comput Biol 9:e1002937PubMedCentralCrossRefPubMed Chen Y, Wang S, Hilgetag CC, Zhou C (2013) Trade-off between multiple constraints enables simultaneous formation of modules and hubs in neural systems. PLoS Comput Biol 9:e1002937PubMedCentralCrossRefPubMed
Zurück zum Zitat Colizza V, Flammini A, Serrano MA, Vespignani A (2006) Detecting rich-club ordering in complex networks. Nat Phys 2:110–115CrossRef Colizza V, Flammini A, Serrano MA, Vespignani A (2006) Detecting rich-club ordering in complex networks. Nat Phys 2:110–115CrossRef
Zurück zum Zitat Csermely P (2006) Weak links: stabilizers of complex systems from proteins to social networks. Springer, Berlin Csermely P (2006) Weak links: stabilizers of complex systems from proteins to social networks. Springer, Berlin
Zurück zum Zitat Cui A, Yang Z, Zhou T (2012) Roles of ties in spreading. arXiv:1204.0100v1 Cui A, Yang Z, Zhou T (2012) Roles of ties in spreading. arXiv:1204.0100v1
Zurück zum Zitat de Reus MA, van den Heuvel MP (2013) Rich club organization and intermodule communication in the cat connectome. J Neurosci 33:12929–12939CrossRefPubMed de Reus MA, van den Heuvel MP (2013) Rich club organization and intermodule communication in the cat connectome. J Neurosci 33:12929–12939CrossRefPubMed
Zurück zum Zitat Ercsey-Ravasz M, Markov NT, Lamy C, Van Essen DC, Knoblauch K, Toroczkai Z, Kennedy H (2013) A predictive network model of cerebral cortical connectivity based on a distance rule. Neuron 80:184–197PubMedCentralCrossRefPubMed Ercsey-Ravasz M, Markov NT, Lamy C, Van Essen DC, Knoblauch K, Toroczkai Z, Kennedy H (2013) A predictive network model of cerebral cortical connectivity based on a distance rule. Neuron 80:184–197PubMedCentralCrossRefPubMed
Zurück zum Zitat Fries P (2005) A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn Sci 9:474–480CrossRefPubMed Fries P (2005) A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn Sci 9:474–480CrossRefPubMed
Zurück zum Zitat Gómez-Gardeñes J, Zamora-López G, Moreno Y, Arenas A (2010) From modular to centralized organization of synchronization in functional areas of the cat cerebral cortex. PLoS One 5:e12313PubMedCentralCrossRefPubMed Gómez-Gardeñes J, Zamora-López G, Moreno Y, Arenas A (2010) From modular to centralized organization of synchronization in functional areas of the cat cerebral cortex. PLoS One 5:e12313PubMedCentralCrossRefPubMed
Zurück zum Zitat Good BH, de Montjoye Y-A, Clauset A (2010) Performance of modularity maximization in practical contexts. Phys Rev E 81:046106CrossRef Good BH, de Montjoye Y-A, Clauset A (2010) Performance of modularity maximization in practical contexts. Phys Rev E 81:046106CrossRef
Zurück zum Zitat Goulas A, Bastiani M, Bezgin G, Uylings HBM, Roebroeck A, Stiers P (2014) Comparative analysis of the macroscale structural connectivity in the macaque and human brain. PLoS Comput Biol 10:e1003529PubMedCentralCrossRefPubMed Goulas A, Bastiani M, Bezgin G, Uylings HBM, Roebroeck A, Stiers P (2014) Comparative analysis of the macroscale structural connectivity in the macaque and human brain. PLoS Comput Biol 10:e1003529PubMedCentralCrossRefPubMed
Zurück zum Zitat Granovetter M (1973) The strength of weak ties. Am J Sociol 78:1360–1380CrossRef Granovetter M (1973) The strength of weak ties. Am J Sociol 78:1360–1380CrossRef
Zurück zum Zitat Harriger L, van den Heuvel MP, Sporns O (2012) Rich club organization of macaque cerebral cortex and its role in network communication. PLoS One 7:e46497PubMedCentralCrossRefPubMed Harriger L, van den Heuvel MP, Sporns O (2012) Rich club organization of macaque cerebral cortex and its role in network communication. PLoS One 7:e46497PubMedCentralCrossRefPubMed
Zurück zum Zitat Herculano-Houzel S, Mota B, Wong P, Kaas JH (2010) Connectivity-driven white matter scaling and folding in primate cerebral cortex. Proc Natl Acad Sci USA 107:19008–19013PubMedCentralCrossRefPubMed Herculano-Houzel S, Mota B, Wong P, Kaas JH (2010) Connectivity-driven white matter scaling and folding in primate cerebral cortex. Proc Natl Acad Sci USA 107:19008–19013PubMedCentralCrossRefPubMed
Zurück zum Zitat Hilgetag CC, Grant S (2010) Cytoarchitectural differences are a key determinant of laminar projection origins in the visual cortex. NeuroImage 51:1006–1017CrossRefPubMed Hilgetag CC, Grant S (2010) Cytoarchitectural differences are a key determinant of laminar projection origins in the visual cortex. NeuroImage 51:1006–1017CrossRefPubMed
Zurück zum Zitat Jones DK, Knösche TR, Turner R (2013) White matter integrity, fiber count, and other fallacies: the do’s and don’ts of diffusion MRI. NeuroImage 73:239–254CrossRefPubMed Jones DK, Knösche TR, Turner R (2013) White matter integrity, fiber count, and other fallacies: the do’s and don’ts of diffusion MRI. NeuroImage 73:239–254CrossRefPubMed
Zurück zum Zitat Kaiser M, Hilgetag CC (2004) Edge vulnerability in neural and metabolic networks. Biol Cybern 90:311–317CrossRefPubMed Kaiser M, Hilgetag CC (2004) Edge vulnerability in neural and metabolic networks. Biol Cybern 90:311–317CrossRefPubMed
Zurück zum Zitat Kaiser M, Hilgetag CC (2006) Nonoptimal component placement, but short processing paths, due to long-distance projections in neural systems. PLoS Comput Biol 2:e95PubMedCentralCrossRefPubMed Kaiser M, Hilgetag CC (2006) Nonoptimal component placement, but short processing paths, due to long-distance projections in neural systems. PLoS Comput Biol 2:e95PubMedCentralCrossRefPubMed
Zurück zum Zitat Kaiser M, Görner M, Hilgetag CC (2007) Criticality of spreading dynamics in hierarchical cluster networks without inhibition. New J Phys 9:110CrossRef Kaiser M, Görner M, Hilgetag CC (2007) Criticality of spreading dynamics in hierarchical cluster networks without inhibition. New J Phys 9:110CrossRef
Zurück zum Zitat Kaiser M, Hilgetag CC, Van Ooyen A (2009) A simple rule for axon outgrowth and synaptic competition generates realistic connection lengths and filling fractions. Cereb Cortex 19:3001–3010CrossRefPubMed Kaiser M, Hilgetag CC, Van Ooyen A (2009) A simple rule for axon outgrowth and synaptic competition generates realistic connection lengths and filling fractions. Cereb Cortex 19:3001–3010CrossRefPubMed
Zurück zum Zitat Markov NT, Ercsey-Ravasz M, Van Essen DC, Knoblauch K, Toroczkai Z, Kennedy H (2013a) Cortical high-density counterstream architectures. Science 342:1238406PubMedCentralCrossRefPubMed Markov NT, Ercsey-Ravasz M, Van Essen DC, Knoblauch K, Toroczkai Z, Kennedy H (2013a) Cortical high-density counterstream architectures. Science 342:1238406PubMedCentralCrossRefPubMed
Zurück zum Zitat Markov NT et al (2013b) The role of long-range connections on the specificity of the macaque interareal cortical network. Proc Natl Acad Sci USA 110:5187–5192PubMedCentralCrossRefPubMed Markov NT et al (2013b) The role of long-range connections on the specificity of the macaque interareal cortical network. Proc Natl Acad Sci USA 110:5187–5192PubMedCentralCrossRefPubMed
Zurück zum Zitat Maslov S, Sneppen K (2002) Specificity and stability in topology of protein networks. Science 296:910–913CrossRefPubMed Maslov S, Sneppen K (2002) Specificity and stability in topology of protein networks. Science 296:910–913CrossRefPubMed
Zurück zum Zitat Moretti P, Muñoz MA (2013) Griffiths phases and the stretching of criticality in brain networks. Nat Commun 4:2521CrossRefPubMed Moretti P, Muñoz MA (2013) Griffiths phases and the stretching of criticality in brain networks. Nat Commun 4:2521CrossRefPubMed
Zurück zum Zitat Onnela J-P, Saramäki J, Hyvönen J, Szabó G, Lazer D, Kaski K, Kertész J, Barabási A-L (2007) Structure and tie strengths in mobile communication networks. Proc Natl Acad Sci U S A 104:7332–7336PubMedCentralCrossRefPubMed Onnela J-P, Saramäki J, Hyvönen J, Szabó G, Lazer D, Kaski K, Kertész J, Barabási A-L (2007) Structure and tie strengths in mobile communication networks. Proc Natl Acad Sci U S A 104:7332–7336PubMedCentralCrossRefPubMed
Zurück zum Zitat Pajevic S, Plenz D (2012) The organization of strong links in complex networks. Nat Phys 8:429–436CrossRef Pajevic S, Plenz D (2012) The organization of strong links in complex networks. Nat Phys 8:429–436CrossRef
Zurück zum Zitat Pérez-Escudero A, De Polavieja GG (2007) Optimally wired subnetwork determines neuroanatomy of Caenorhabditis elegans. Proc Natl Acad Sci USA 104:17180–17185PubMedCentralCrossRefPubMed Pérez-Escudero A, De Polavieja GG (2007) Optimally wired subnetwork determines neuroanatomy of Caenorhabditis elegans. Proc Natl Acad Sci USA 104:17180–17185PubMedCentralCrossRefPubMed
Zurück zum Zitat Santarnecchi E, Galli G, Polizzotto NR, Rossi A, Rossi S (2014) Efficiency of weak brain connections support general cognitive functioning. Hum Brain Mapp. doi:10.1002/hbm.22495 PubMed Santarnecchi E, Galli G, Polizzotto NR, Rossi A, Rossi S (2014) Efficiency of weak brain connections support general cognitive functioning. Hum Brain Mapp. doi:10.​1002/​hbm.​22495 PubMed
Zurück zum Zitat Scannell JW, Blakemore C, Young MP (1995) Analysis of connectivity in the cat cerebral cortex. J Neurosci 15:1463–1483PubMed Scannell JW, Blakemore C, Young MP (1995) Analysis of connectivity in the cat cerebral cortex. J Neurosci 15:1463–1483PubMed
Zurück zum Zitat Shu P, Tang M, Gong K, Liu Y (2012) Effects of weak ties on epidemic predictability in community networks. arXiv:1207.0931v1 Shu P, Tang M, Gong K, Liu Y (2012) Effects of weak ties on epidemic predictability in community networks. arXiv:1207.0931v1
Zurück zum Zitat Sporns O, Tononi G, Edelman GM (2000) Theoretical neuroanatomy: relating anatomical and functional connectivity in graphs and cortical connection matrices. Cereb Cortex 10:127–141CrossRefPubMed Sporns O, Tononi G, Edelman GM (2000) Theoretical neuroanatomy: relating anatomical and functional connectivity in graphs and cortical connection matrices. Cereb Cortex 10:127–141CrossRefPubMed
Zurück zum Zitat ter Wel M, Tiesinga P (2012) Phase shifting in a network of cortical circuits and its implications for communication through coherence. Society for Neuroscience, New Orleans, LA. Program/poster 673.11/FF20 ter Wel M, Tiesinga P (2012) Phase shifting in a network of cortical circuits and its implications for communication through coherence. Society for Neuroscience, New Orleans, LA. Program/poster 673.11/FF20
Zurück zum Zitat van den Heuvel MP, Sporns O (2013a) Network hubs in the human brain. Trends Cog Sci 17:683–696CrossRef van den Heuvel MP, Sporns O (2013a) Network hubs in the human brain. Trends Cog Sci 17:683–696CrossRef
Zurück zum Zitat van den Heuvel MP, Sporns O (2013b) An anatomical substrate for integration among functional networks in human cortex. J Neurosci 33:14489–14500CrossRefPubMed van den Heuvel MP, Sporns O (2013b) An anatomical substrate for integration among functional networks in human cortex. J Neurosci 33:14489–14500CrossRefPubMed
Zurück zum Zitat Vértes PE, Alexander-bloch AF, Gogtay N, Giedd JN, Rapoport JL (2012) Simple models of human brain functional networks. Proc Natl Acad Sci USA 109:5868–5873PubMedCentralCrossRefPubMed Vértes PE, Alexander-bloch AF, Gogtay N, Giedd JN, Rapoport JL (2012) Simple models of human brain functional networks. Proc Natl Acad Sci USA 109:5868–5873PubMedCentralCrossRefPubMed
Zurück zum Zitat Von Bonin GV, Bailey P (1947) The neocortex of macaca mulatta. The University of Illinois Press, Urbana Von Bonin GV, Bailey P (1947) The neocortex of macaca mulatta. The University of Illinois Press, Urbana
Zurück zum Zitat Womelsdorf T, Schoffelen J-M, Oostenveld R, Singer W, Desimone R, Engel AK, Fries P (2007) Modulation of neuronal interactions through neuronal synchronization. Science 316:1609–1612CrossRefPubMed Womelsdorf T, Schoffelen J-M, Oostenveld R, Singer W, Desimone R, Engel AK, Fries P (2007) Modulation of neuronal interactions through neuronal synchronization. Science 316:1609–1612CrossRefPubMed
Zurück zum Zitat Zhao M, Zhou C, Lü J, Lai CH (2011) Competition between intra-community and inter-community synchronization and relevance in brain cortical networks. Phys Rev E 84:016109CrossRef Zhao M, Zhou C, Lü J, Lai CH (2011) Competition between intra-community and inter-community synchronization and relevance in brain cortical networks. Phys Rev E 84:016109CrossRef
Zurück zum Zitat Zingg B, Hintiryan H, Gou L, Song MY, Bay M, Bienkowski MS, Foster NN, Yamashita S, Bowman I, Toga AW, Dong H-W (2014) Neural networks of the mouse neocortex. Cell 156:1096–1111PubMedCentralCrossRefPubMed Zingg B, Hintiryan H, Gou L, Song MY, Bay M, Bienkowski MS, Foster NN, Yamashita S, Bowman I, Toga AW, Dong H-W (2014) Neural networks of the mouse neocortex. Cell 156:1096–1111PubMedCentralCrossRefPubMed
Metadaten
Titel
The strength of weak connections in the macaque cortico-cortical network
verfasst von
Alexandros Goulas
Alexander Schaefer
Daniel S. Margulies
Publikationsdatum
01.09.2015
Verlag
Springer Berlin Heidelberg
Erschienen in
Brain Structure and Function / Ausgabe 5/2015
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-014-0836-3

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